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Biological Effects of Bacterial Lipopolysaccharide

Biological Effects of Bacterial Lipopolysaccharide

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REVIEW
Biological effects of bacterial lipopolysaccharide(endotoxin) in fish: A review
P. Swain*, S.K. Nayak, P.K. Nanda, S. Dash
Fish Health Management Division, Central Institute of Freshwater Aquaculture,Kausalyaganga, Bhubaneswar 751 002, Orissa, India
Received 24 December 2007; revised 2 April 2008; accepted 18 April 2008Available online 26 April 2008
KEYWORDS
Biological effects;Endotoxin;Fish;Gram-negativebacteria;Lipopolysaccharide
Abstract
Bacterial lipopolysaccharides (LPS), also termed endotoxins, considered to bea major virulence factor, are responsible for the lethal effects and clinical manifestations ofdiseases in humans and animals. Higher animals are extremely sensitive to endotoxin evenat low doses but lower vertebrates like fish are often resistant to endotoxic shock. Toll-like re-ceptor (TLR)-4 is mainly involved in the activation of the immune system by LPS through thespecific recognition of its endotoxin (Lipid A) moiety. Although several Toll-like receptorsare present in fish, those molecules specifically involved in TLR-4 mediated endotoxinrecognition have not been fully established in different fish species. Despite this, LPS hasthe potency to express cytokines, acute-phase proteins and also exerts immunological, path-ological, physiological, immuno-endocrinological and neuro-immunological effects in severalfish species. The immunostimulating effects of endotoxin by triggering various immune para-meters such as Tand B lymphocytes, macrophages, and complement systems have been estab-lished in teleosts. This article reviews the multiple biological effects of endotoxin which willfurther strengthen the knowledge among researchers on various aspects of endotoxin in lower vertebrates, particularly in the piscine system.
ª
2008 Elsevier Ltd. All rights reserved.
Introduction
Endotoxins, the non-secreted cell membrane inherenttoxins, are capable of producing toxic manifestations inthe host resulting in strong innate inflammatoryresponses. They are considered to be the major virulencefactor for several Gram-negative bacteria, and areresponsible for the lethal effects and clinical manifesta-tions of diseases in humans and animals[1
e
4]. The effectsof Gram-negative bacterial infections and/or endotoxin inchronic cases are often deleterious as compared to acutecases[5].
* Corresponding author. Tel.:
þ
91 943 723 1099; fax:
þ
91 674 2465407.
E-mail address:
pswainy2k@yahoo.co.in(P. Swain).1050-4648/$ - see front matter 
ª
2008 Elsevier Ltd. All rights reserved.doi:10.1016/j.fsi.2008.04.009
available at www.sciencedirect.comjournal homepage:www.elsevier.com/locate/fsi
Fish & Shellfish Immunology (2008)
25
, 191
e
201
 
Endotoxins are the complex lipopolysaccharide compo-nents of the outer cell wall membrane of Gram-negativebacteria. They are usually large molecular weight sub-stances with unique chemical structure, consisting of threeregions, i.e., an outer polysaccharide region (commonlyknown as ‘O’ antigen, a linear or branched component ofoligosaccharide residues), a unique polysaccharide coreregion (consisting of short chain sugars), and an inner fattyacid rich region (i.e., Lipid A containing diglucosamine unitwith long-chain fatty acids) (Fig. 1). The polysaccharidemoiety is mainly responsible for serological specificity whilethe Lipid A moiety determines biological functions[6
e
8].The Lipid A components are found to be uniform in differ-ent Gram-negative bacteria, but their potency and spec-trum of action differ from each other [9].The prototypical name of endotoxin is lipopolysaccha-ride (LPS), which is the cell wall component of most of theGram-negative bacteria. However, Gram-positive bacterialike
Listeria monocytogenes
also possess endotoxin-like ac-tivity[10]. Although the term ‘endotoxin’ is commonlyused, it is often referred to by synonymous terms like pyro-gen, LPS, or biovin antigen[11]. In aquaculture, LPS is themost commonly used terminology.Higher animals are extremely sensitive to endotoxineven at low doses but lower vertebrates such as frog andfish are stated to be resistant to endotoxic shock[12].However, endotoxin/LPS has been found many times tobe responsible for the pathogenicity of several bacterialdiseases, especially of Gram-negative origin, in fish[13].Therefore, this review elucidates the basic mechanismthrough which endotoxin interacts by manifesting multiplebiological effects in different fish species. This will further strengthen the knowledge among researchers on variousaspects and mechanism of action of endotoxin in lower vertebrates, particularly in fish.
Biological activity of endotoxin
Endotoxin can induce innumerable biological effects in allliving systems. No other natural product is known to elicitsuch a great diversity of reaction as endotoxins do[11].Common endotoxic effects include shock, pyrogenicity,hypotension, neutropenia, intravascular coagulation, hypo-ferraemia, leucocytosis, leucopenia, sepsis and abortion[14
e
21]. In a host it affects the cellular and humoral immu-nity, carbohydrate and lipid metabolisms, and haematolog-ical parameters. However, these physiological andbiochemical responses vary depending upon species andthe doses of the endotoxin. But at higher doses it couldbe lethal to any animal.In several aquatic species including fish, it exertsmultiple responses like immunological, pathological, phys-iological, immuno-endocrinological and neuro-immunologi-cal effects[22
e
34]. The common effects of endotoxin ondifferent fish species are summarized inTable 1. However,many times these responses are qualitatively different inlower vertebrates than in higher vertebrates. In mammals,depletion of liver glycogen, depression of liver tryptophanpyrrolase activity, instant decline in arterial pressure,abrupt reduction of heart rate and severe hypotension arecommon metabolic derangements observed in response toendotoxin[47]. But fishes often do not respond in a similar manner to mammals. For example, yearlings of cohosalmon (
Oncorhynchus kisutch
) and rainbow trout (
Onco-rhynchus mykiss
), when injected with endotoxin, did notshow any cardiovascular response or effect on liver trypto-phan pyrrolase activity except depletion of liver glycogenlevel[47]. Similarly, in juveniles of salmon (
Salmo salar 
),significant decrease in the heart rate from 4th day onwardsafter an initial increase in response to LPS was observed byEddy[38].
Endotoxicity and clinical effectsof endotoxin in fish
Endotoxic shock is a common problem in humans andanimals due to Gram-negative bacterial infection. Higher vertebrates like cat, rabbit, guinea pig, dog, calf, swineand human are very sensitive to endotoxic shock whereaslower vertebrates like fish and frog are resistant to it[47,48]. Fishes like
O. kisutch
and
O. mykiss
are reportedto be resistant to
Escherichia coli
and
Aeromonas salmoni-cida
endotoxins for doses up to 80 mg kg
À
1
body weight[47]. Similarly, a tropical fish like Indian major carp,
Labeorohita
, is also found to resist endotoxin to a dose of 20 EUper fish without showing any abnormality[33].Endotoxin exerts several clinical signs and symptomssuch as hyperaemia or discolouration of mucus membrane,hypotension, altered capillary refill time, acute disruptionof gastric, small and large intestine motility resulting indecreased gastrointestinal sound, increased body temper-ature, heart and respiratory rates, and dehydration in anysensitive individual[49,50]. However, the clinical signs andsymptoms may vary depending upon the type, previous ex-posure and dose of the toxin. In fish, upon administrationof endotoxin even at high doses, no clinical signs, changesin body colouration, abnormalities and behaviouralchanges could be recorded[33,47], although it could bea potent anorexic agent for fish which can reduce the ap-petite by influencing gene expression of appetite relatedneuropeptide[51].In an aquatic environment, fish are not only intimatelyassociated with Gram-negative bacteria but are also
Figure 1
A typical lipopolysaccharide unit showing differentregions.
192 P. Swain et al.
 
Table 1
In vivo
effects of endotoxin in different fish speciesSl. No Fish LPS/Source Mode of administration Effects/Activity References1
D. rerio E. coli
Immersion Enhances the production of cytokines TNF-
a
,IL-1
b
L. rohita E. coli
Intraperitoneal @1 EU fish
À
1
Increases lysozyme, total globulin level,myeloperoxidase and respiratory burstactivities[33]
L. rohita E. coli
Intraperitoneal @10 EU fish
À
1
Decreases lysozyme, total globulin level,myeloperoxidase and respiratory burstactivities[33]3
P. flavescens
LPS Intraperitoneal @3 mg kg
À
1
body weightIncreases cortisol level[35]4
G. morhua A. salmonicida
Bath/Feed treatment Increases survivability[36]5
C. carpio
LPS Immunization @ LPS 50/1250
m
g fish
À
1
Increases phagocytic activity, phagocytic indexof macrophages and Ig level[37]6
S. salar 
LPS Injection Decreases heart rate after 4 days[38]7
S. salar 
LPS Bath (0.25% LPS
þ
1%glucan)Increases lysozyme of head kidney, intestine,macrophages and polymorphonuclear cells[39]8
O. mossambicus E. coli
(0111:B4)
In vivo
Increases plasma free fatty acid, cortisol level[25]9
O. mossambicus E. coli
(0111:B4)
In vivo
Releases adenocorticotropic hormone,
a
-MSH[24]10
O. mossambicus E. coli
Injection Increases CRH and
a
-MSH content. No change incortisol level[5]11
C. carpio
10
m
g ml
-1
LPS
þ
100
m
g
b
- glucan Intraperitoneal Increases neutrophils, monocytes count[32]0.25% LPS
þ
1% glucan Oral No change in relative percentage of survival100
m
g ml
-1
LPS
þ
1000
m
g
b
- glucan Bath No change in relative percentage of survivalLPS (10
m
g)
þ
b
- glucan (100
m
g) Intraperitoneal 100% relative percentage of survival12
S. aurata E. coli
Bath Increases anti protease activity containingprotease inhibitors
a
1 and 2, anti- plasmin,
a
2macroglobulin. Enhances protection against
Photobacterium damsela
[40]13
S. salar A. salmonicida
Immunization Enhances specic antibody level[41]14
O. mykiss A. salmonicida
Intraperitoneal @50
m
g fish
À
1
Increases antibody titre which persists upto 2
e
4 weeks[42]
 A. salmonicida
þ
Liposome Intraperitoneal @50
m
g fish
À
1
Increases antibody titre which persistsup to 6
e
14 weeks15
S. salar 
LPS
In vivo
Enhances phagocytosis, pinocytic activity,production of intracellular superoxidase anion[43]16
O. mykiss
LPS
In vivo
Induces hypoferremic responses[44]17
C. carpio A. hydrophila
Dip immunization Enhances survivability. No specific antibodylevel[45]18
O. mykiss A. salmonicida
/
E. coli
(055 B5) Intravascula@ 25 mg kg
À
1
Elevates cortisol level[46]
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